57
The Journal of Experimental Biology 199, 57–64 (1996)
Printed in Great Britain © The Company of Biologists Limited 1996
JEB0128
METABOLIC CONSTRAINTS ON LONG-DISTANCE MIGRATION IN BIRDS
MARCEL KLAASSEN
Centre for Limnology, Netherlands Institute of Ecology, Rijksstraatweg 6, NL-3631 AC Nieuwersluis,
The Netherlands
Summary
The flight range of migrating birds depends crucially on
the amount of fuel stored by the bird prior to migration or
taken up en route at stop-over sites. However, an increase
in body mass is associated with an increase in energetic
costs, counteracting the benefit of fuel stores. Water
imbalance, occurring when water loss exceeds metabolic
water production, may constitute another less well
recognised problem limiting flight range. The main route
of water loss during flight is via the lungs; the rate of loss
depends on ambient temperature, relative humidity and
ventilatory flow and increases with altitude. Metabolite
production results in an increased plasma osmolality, also
endangering the proper functioning of the organism during
flight. Energetic constraints and water-balance problems
may interact in determining several aspects of flight
behaviour, such as altitude of flight, mode of flight, lap
distance and stop-over duration. To circumvent energetic
and water-balance problems, a bird could migrate in short
hops instead of long leaps if crossing of large ecological
barriers can be avoided. However, although necessitating
larger fuel stores and being more expensive, migration by
long leaps may sometimes be faster than by short hops.
Time constraints are also an important factor in explaining
why soaring, which conserves energy and water, occurs
exclusively in very large species: small birds can soar at low
speeds only. Good navigational skills involving accurate
orientation and assessment of altitude and air and ground
speed assist in avoiding physiological stress during
migration.
Key words: migration, energetics, water balance, fuel stores, time
minimization, allometric relationships, flight altitude, navigation,
birds.
Introduction
‘What intensity and gladness of life was in it, what a
wonderful inherited knowledge in its brain, and what an
inexhaustible vigour in its slender frame to enable it to perform
that annual double journey of upwards of ten thousand miles!’
Not only Hudson (1939; here expressing his excitement about
the migratory ability of the upland sandpiper Bartramia
longicauda) but many other ornithologists have realized for
years that birds need brains as well as muscles to conduct a
long-distance migratory journey successfully. In this review, I
focus on the latter and discuss a few physiological
characteristics that probably greatly determine and constrain
the behaviour of migrating birds. Finally, I discuss the impact
of our knowledge of navigation on ecophysiological studies of
bird migration in the conviction that good navigational skills
will alleviate the impact of physiological constraints for
migrants.
Necessity of fuel stores
Migratory birds often have to cross large areas, such as
deserts and oceans, without a suitable habitat for fuelling.
Before such inhospitable areas can be passed, body stores have
to be build up to fuel the energetically costly flight (e.g.
Pennycuick, 1975, 1989; Masman and Klaassen, 1987). In
long-distance migrants, body mass may more than double prior
to migration. However, apart from ecological barriers, time
constraints can also explain the accumulation of fuel stores for
migration. Ultimately, the total amount of fuel stores is
probably a trade-off between the effects of fuel stores on the
energetics, duration and risks of migration.
Time constraints act simply because seasons are of limited
duration. Moreover, early arrival may be rewarded with a
higher competitiveness for limiting resources (von Haartman,
1968). But why does this make it so important for a timeminimising migrant to build up fuel stores? For a number of
possible reasons (Hansson and Petterson, 1989; Klaassen and
Biebach, 1994) the rate of refuelling is initially low upon
arrival at a stop-over site. During the first few days, the migrant
may even loose some weight. These problems during settling
reduce the speed of migration and favour a reduction of the
number of stop-overs. Consequently, fuel stores are increased.
Variability in the quality of refuelling sites also influences the
size of stores. When a bird happens to find a relatively good
refuelling site, it uses the opportunity to build up larger fuel
stores than on average sites. Moreover, as a bird cannot foresee
the situation on the staging sites to come, it builds up some
extra fuel to reduce the risk of starvation. Thus, variation in
site quality also determines the amount of fuel stored.
M. KLAASSEN
Allometric considerations in relation to fuel loads
Size-dependent physiological problems may occur in
relation to migration. For instance, when large migratory birds
(are forced to) use flapping flight, they face larger energetic
problems than smaller birds. Fuel loads are limited by the
morphological capabilities of birds; above a certain threshold,
birds will not be able to take off (Hedenström and Alerstam,
1992). Maximum fuel-carrying capacity (the ratio of total body
mass to lean body mass, hmax) decreases with body mass
(Hedenström and Alerstam, 1992; Fig. 1A). Because flight
range increases almost linearly with fuel load (Fig. 1B),
maximum flight range will also decrease with body mass.
Thus, when covering a certain distance between the summer
and winter areas with maximum fuel load, large birds will have
to refuel more frequently than small birds. As mentioned
earlier, each stop-over normally involves some time loss
because the rate of refuelling is initially low. At the staging
site, large birds face another energetic problem that limits their
speed of migration: their maximum rate of fuel deposition is
relatively low. This is the result of a more or less universal
maximum limit to the daily metabolizable energy intake
(Kirkwood, 1983). On theoretical grounds, maximum fuel
deposition rate is expected to scale to body mass with an
exponent of 20.27, a value that is largely supported by
empirical data (Lindström, 1991; Fig. 2).
Thus, the larger the migratory bird, the larger the energetic
problems it faces when using flapping flight. Soaring is
energetically much cheaper and could be a good alternative to
flapping flight if the bird is energy-constrained. Moreover,
large birds have a relatively high soaring speed, making
soaring a good alternative to flapping flight not only to
conserve energy but also to save time (Pennycuick, 1989;
Hedenström, 1993). It is not only their typically low soaring
speed that makes soaring a poor alternative for timeconstrained small migratory birds. Small birds will also be
blown off course easily when soaring at low speeds
(Hedenström, 1993). At temperate latitudes, thermal
convection is only available during part of the day. This results
in a restricted daily period when migration by soaring flight is
possible. Therefore, with an increase in latitude, large species
increasingly use flapping instead of soaring flight
(Hedenström, 1993).
Composition of fuel stores
To maximise flight range at the lowest possible costs, fat is
the preferred fuel for flight. Fat is the most energy-dense
metabolite and can be synthesised from any type of food that
is digested. Indeed, body stores of migratory birds were long
thought to consist almost entirely of fat (Connell et al. 1960;
Odum et al. 1964, 1965), but evidence is continuously
accumulating that the synthesis of protein is often also
involved (Piersma, 1990). Studies on the composition of body
stores for migration using carcass analyses may provide insight
into the nature of these tissues. After having noted that many
earlier studies were flawed as a result of methodological
3
A
hmax
However, with an increase in fuel stores, flight costs in
energy per unit distance increase rapidly (Pennycuick, 1975,
1989). Besides the increased energetic costs with increasing
fuel load, other types of costs might also exist that migrants
may take into account in determining their optimal fuel load.
These other costs could include increases in the risks of injury,
illness and predation and a decrease in foraging efficiency (for
a review, see Witter and Cuthill, 1993). These considerations
suggest that fuel stores must be kept at the lowest possible level
and that the migratory journey must be undertaken in short
hops rather than long leaps. On the basis of these arguments,
several theoretical models have been developed to explain the
size of fuel stores in migrants (Alerstam and Lindström, 1990;
Gudmundsson et al. 1991; Lindström and Alerstam, 1992;
Weber et al. 1994, 1995; Klaassen and Lindström, 1996).
These models have emphasized the need for more empirical
data on the costs and benefits of fuel stores.
1
0.01
0.1
1
10
Lean body mass (kg)
B
Maximum range (km)
58
6000
4000
2000
0
1
2
hmax
3
Fig. 1. (A) Calculated maximum fuel-carrying capacities (ratio of
total body mass to lean body mass, hmax; filled symbols) for 15 species
of birds with known aerodynamic characteristics as a function of lean
body mass. In addition, maximum observed fuel-carrying capacities
in 41 species of free-living birds (open symbols) in relation to lean
body mass are presented. (B) Calculated maximum flight range
according to Pennycuick (1989) as a function of calculated maximum
fuel-carrying capacities for the 15 species of birds with known
aerodynamic characteristics. Least-squares regression lines are drawn
(A, r2=0.431, P<0.01; B, r2=0.874, P<0.01). Data from Hedenström
and Alerstam (1992).
Metabolic constraints on long-distance migration in birds
Fuel deposition rate
(% of lean body mass per day)
14
12
10
8
6
4
2
0
1
10
100
Lean body mass (g)
1000
Fig. 2. Maximum fuel deposition rates (percentage of daily mass
increase relative to lean body mass) in migrating birds of different
sizes. From top to bottom the three lines depict the predicted
maximum fuel deposition rate for non-passerines, shorebirds and
passerines, respectively, based on allometric considerations.
Observed maximum fuel deposition rates of populations (open
symbols) and individuals in the field (filled symbols) are presented
for passerines (triangles), non-passerines (squares) and shorebirds
(circles). From Lindström (1991) (reprinted with permission).
inconsistencies, Lindström and Piersma (1993) re-evaluated
the available data and found strong indications that birds
generally, but not always, deposit protein before take-off.
Recalculating data for bar-tailed godwit Limosa lapponica
(Piersma and Jukema, 1990), Lindström and Piersma (1993)
estimated that migratory fuel stores consist of 35 % non-fat
components (probably protein with associated water). By
accurately measuring the energy balance of individual birds
and relating the difference between metabolizable energy
intake and energy expenditure to changes in body mass, the
energy density of fuel stores, and hence their composition, can
be determined. Such a method, although it can unfortunately
only be used in birds kept under laboratory conditions, does
not suffer from the methodological problems outlined by
Lindström and Piersma (1993) for carcass analyses. In three
migratory bird species, this method has been used to evaluate
the composition of fuel stores during the migratory period,
yielding values for fat content in the range 71–82 % (Klaassen
et al. 1990; Klaassen and Biebach, 1994; M. Klaassen, Å.
Lindström and R. Zijlstra, in preparation). Again, more support
for body stores containing a mixture of protein and fat comes
from nitrogen balance studies in both migratory (M. Klaassen,
Å. Lindström and R. Zijlstra, in preparation) and nonmigratory birds (Lindgård et al. 1992, and studies cited
therein). These nitrogen balance studies revealed that the fat
content of fuel stores ranged between 62 and 81 %. Finally,
Jenni-Eiermann and Jenni (1991) found elevated levels of uric
acid in the blood of actively migrating passerines at a high
mountain pass in the Swiss Alps, which is an unambiguous
indication that protein, as well as fat, is catabolized during
migration.
59
Studies of muscle mass in relation to the accumulation of
body fat for migration show adaptive increases in muscle size,
while composition and function are similar on a mass-specific
basis (Kendall et al. 1973; McLandress and Raveling, 1981;
Marsh, 1983, 1984). These increases in flight muscle mass for
migration are generally thought to be necessary to carry the
extra weight of body stores (Pennycuick, 1975; Marsh and
Storer, 1981; Dawson et al. 1983). It is possible that it is this
extra muscle mass in migratory birds that is reflected in the
18–38 % wet protein (i.e. protein plus associated water, which
normally occur in the ratio 3:7) in the body stores. It is also
possible that the proteins are stored in active tissue other than
muscles to support the higher metabolic demands of a bird with
a high fuel load. Alternatively, or additionally, it might be
impossible for an animal to function normally without some
protein utilisation or turnover.
Whatever the reason for storing a mixture of fat and protein,
rather than just fat, the important consequence of this for a
migratory bird is its impact on maximum flight range. 1 g of
tissue containing, for example, 75 % fat and 25 % wet protein
yields 22 % less energy than 1 g of pure fat. The distance a
migratory bird can cover with the fat/protein mixture is thus
also 22 % shorter than it could cover if it had been catabolizing
fat exclusively.
Problems of water
The necessity for migratory birds to balance their energy
budget is obvious. However, we should not oversimplify the
matter. Apart from fat and protein, there are further body
resources that are burdened under the extreme effort of longdistance migration. Water imbalance may also limit a bird’s
flight range (Carmi et al. 1992). I will discuss (1) the routes of
water gain and loss, which are very different from those of
energy, and (2) evidence that problems of water balance
participate in governing migratory behaviour.
When crossing seas and deserts, a bird’s water budget must
be carefully balanced because no fresh water is available for
rehydration. However, when crossing less inhospitable areas,
intermittent stop-overs to rest, drink or eat should also be
avoided because they are costly events, especially when
cruising at high altitude. Reaching these high air layers is
energetically expensive (Hedenström and Alerstam, 1992).
When heat-stressed, birds use water for evaporative cooling.
Under such circumstances, a bird may rapidly dehydrate. Even
under thermoneutral conditions or when cold-stressed,
dehydration may easily follow from passive water loss. Most
water is lost via the lungs. Inhaled ambient air is brought to
body temperature and saturated with water. During exhalation,
the air is cooled down, causing condensation of water vapour
and recovery of water that was added to the air upon inhalation.
However, the exhaled air temperature is still well above the
inhaled air temperature (Berger et al. 1971) and the inhaled air
is rarely saturated with water, in contrast to the exhaled air,
resulting in a net loss of water.
During flight, both fat and proteins are catabolized as
60
M. KLAASSEN
discussed above. The consequent increase in levels of uric acid
and other plasma metabolites, possibly in concert with some
dehydration, will result in an increased blood plasma
osmolality, endangering the proper functioning of the
organism.
With an increase in flight altitude, partial oxygen pressure
drops, leading to an increase in the ventilatory flow through
the lungs and a concomitant increase in water loss. Water loss
may be balanced by water production. For example, catabolism
of fat alone yields 27 ml H2O kJ21. When catabolizing a
mixture of 70 % fat and 30 % wet protein, the water yield is
somewhat more favourable at 34 ml H2O kJ21.
Using physiological models of energy expenditure and water
loss (Fig. 3), it has become clear that problems of water
balance may indeed occur during crossings of the Sahara desert
(Carmi et al. 1992; Klaassen, 1995; M. Klaassen and H.
Biebach, in preparation). However, a deficit in water balance
may also occur at higher latitudes. This deficit will be most
noticeable in large birds that migrate using flapping flight. For
example, the mute swan Cygnus olor (approximately 10 kg)
has an estimated flight cost of 70 times its basal metabolic rate
(Pennycuick, 1989) and is thus expected to have a high
pulmonary flow. However, although measured at rest only, the
mute swan appears to have a very low breathing frequency,
high oxygen extraction and large tidal volume (Bech and
Johansen, 1980). These characteristics will help mute swans to
avoid water balance deficits during flight. Nevertheless, field
observations on similarly sized and closely related whooper
swans Cygnus cygnus make it conceivable that swans may still
encounter water balance problems during migratory flight.
Using a satellite transmitter, Colin Pennycuick (personal
communication) was able to follow the flight path of a whooper
swan migrating in 1 day from Iceland to Scotland. The bird
flew at very low altitude, practically skimming the tops of the
waves (humid and oxygen-rich air!). Nevertheless, the first
thing that this individual was observed to do upon arrival in
Scotland was to drink large amounts of water.
Interaction between energy and water constraints
Assuming that ambient temperatures at ground level are low
enough to avoid heat stress, water balance problems normally
increase with altitude; although ambient temperature
decreases, along with exhaled air temperature (low water
vapour pressure), this decrease normally cannot compensate
for the increase in pulmonary flow with reduced partial
pressure of oxygen. Energetic costs of flight change little with
altitude. Drag decreases, but the mechanical output needed to
generate lift makes flight a slightly more costly enterprise at
high than at low altitude. Wind assistance is generally regarded
as being of major importance during long-distance migration
(e.g. Alerstam, 1990; Piersma and Jukema, 1990; Piersma and
van de Sant, 1992; Gudmundsson, 1993; Bruderer et al. 1995).
It may be that, at altitudes where favourable winds prevail,
conditions for the maintenance of water balance may be poor.
During autumn migration over the western Sahara desert in
Egypt, favourable conditions for both energy and water
balance prevail at relatively low altitude between 250 and
750 m during the night (Biebach and Klaassen, 1994; M.
Klaassen and H. Biebach, in preparation; Fig. 4). During
spring migration, conditions are expected to be less favourable
for the migrants from a water balance perspective. Although
temperatures are somewhat lower, which is more favourable
for water balance, good wind conditions are usually to be found
only at high altitudes. M. Klaassen and H. Biebach (in
preparation) did not conduct measurements during spring.
However, assuming identical meteorological conditions during
spring and autumn and only reversing migratory direction
resulted in a predicted optimal flight altitude from an energetic
point of view of 3000 m. Taking the water balance into
Energy
Fig. 3. Model used to estimate flight ranges of
migratory birds. The model allows the calculation of
flight range on the basis of limited fuel stores only,
assuming that net water loss equals zero (i.e. the righthand side of the model is not relevant). Alternatively,
both alterations in energy and water budget can be
considered simultaneously, requiring additional input
of variables. For a detailed explanation see Carmi et al.
(1992) and Klaassen (1995).
Water
Input:
pre-flight fat content
wingspan
wind conditions
flight altitude
Additional input:
pre-flight water content
relative humidity
ambient temperature
Energy expenditure
(Pennycuick, 1989)
Respiratory water loss
Body mass
Metabolic water
production
Limits to flight range
imposed by energy
Total water loss
Net water loss
Limits to flight range
imposed by water
Metabolic constraints on long-distance migration in birds
consideration, the optimal flight altitude was predicted to be
only 1750 m (Fig. 4). Unlike the situation in autumn, we thus
expect a conflict between optimisation of energy balance and
water balance in spring.
Bruderer et al. (1995) measured meteorological conditions
and altitudinal distribution of migratory birds crossing the
Negev desert in both spring and autumn. In accordance with
M. Klaassen and H. Biebach’s (in preparation) prediction of a
conflict between energy balance and water balance
considerations in spring, but not in autumn, Bruderer et al.
(1995) found a clear peak in migratory altitude in autumn and
a rather uniform distribution in spring. Unlike M. Klaassen and
H. Biebach’s (in preparation) use of a physiological model to
integrate the impact of various meteorological parameters on
flight range, Bruderer et al. (1995) linked the raw
meteorological data and simple derivatives thereof to
altitudinal distribution, neglecting the rather complicated
interplay between the various variables. They found a high
correlation between tail-wind velocity and altitudinal
distribution in autumn. Interestingly, the fit with tail-wind
61
velocity was poorer in spring, and the significant effect of
temperature indicated a certain preference of the birds to fly at
low altitudes (oxygen-rich air; lower pulmonary flow).
Navigation and physiological constraints
Clearly, good navigational skills will alleviate the impact of
physiological constraints for migrants and vice versa (Fig. 5).
These navigational skills do not necessarily involve finding the
shortest way to the destination. Sometimes physiological
difficulties may be avoided by taking a roundabout way. In
particular, many soaring birds avoid crossing long stretches of
water because of the lack of thermal updraughts at these sites.
White storks Ciconia ciconia show a migratory divide: those
breeding west and east of 11 ˚ E migrate southwest and
southeast, respectively (Cramp and Simmons, 1977). These
two distinct innate migratory directions result in their crossing
the Mediterranean over only narrow stretches of water in two
unusually narrow fronts, across the Strait of Gibraltar and
around the coasts of Levant. Another example is the blackcap
Autumn
Spring
A
Relative migratory
density (%)
50
30
20
10
0
Flight range energy
B
3
2
10−3 × mean flight range (km)
Fig. 4. Comparison of nocturnal
migration over the western Sahara
desert, Egypt, in autumn and spring.
(A) Relative migratory density
(mean + S.D., N=133) measured by
radar in relation to altitude in
autumn. Absolute migratory density
was 7.45 birds m21 h21 on average.
(B,C) Mean flight range (+ S.D.,
N=14)
for
willow
warbler
Phylloscopus trochilus in relation to
altitude (in categories of 250 m)
calculated from weather balloon
measurements in autumn using both
the energy model (B) and the energyand-water model (C). The left-hand
panels depict predictions for
autumnal migration and the righthand panels predictions for vernal
migration. The vernal predictions
were calculated on the basis of the
meteorological conditions measured
in autumn but assuming south-tonorth instead of north-to-south
migration. From M. Klaassen and H.
Biebach (in preparation).
40
1
0
Flight range energy and water
C
3
2
1
0
0
1
2
3
4
>4 0
Altitude (km)
1
2
3
4
>4
62
M. KLAASSEN
Fig. 5. Checklist of points of consideration a
migrant bird has to consider successively before
departing on a long-distance flight. Points
indicated with an open circle refer to constraints
of energy and water balance, those with squares
to navigational considerations. A correct
seasonal timing of departures (triangle) is an
additional important prerequisite. From Piersma
et al. (1990) (reprinted with permission).
Sylvia atricapilla. In this species, migratory behaviour varies
from resident to long-distance migratory (Cramp, 1992). Like
the situation in storks, long-distance migratory blackcaps
breeding west of 12 ˚ E longitude migrate southwest and those
breeding to the east migrate southeast. When reaching Africa,
the southeast migrants continue to migrate towards the south
and southwest. Orientation studies in blackcaps from eastern
Austria have confirmed that the change in migratory direction
is innate and coupled to a time programme. In September and
October, these birds migrate southeast, and they change
migratory direction towards the southwest in November
(Helbig, 1991). Consequently, both storks and blackcaps, as
well as many other bird species, not only avoid crossing the
Mediterranean Sea, but also brush past the inhospitable centre
of the Sahara desert.
I have emphasised that migrants locate air layers where both
favourable winds and meteorological conditions that conserve
water prevail. In addition, birds choose their flight speed
depending on the amount of tail wind; with increasing tail
wind, air speed is reduced so that available stores for migration
are used optimally (Hedenström and Alerstam, 1995).To reach
the optimal altitude, to remain there and to fly at the
energetically optimal speed, special navigational skills are
required. As long as a bird can assess and integrate its air speed
and its position with respect to the ground in all three
dimensions, there is no problem. Visual cues can be used
during the day, but what do birds use at night or when flying
at high altitude? Proposed cues are the change in wind velocity
and direction with height (Elkins, 1988), which could possibly
be measured by airflow sensors in the wings (Brown and
Fedde, 1993), barometric pressure, cloud formation, wind
speed at low altitude or the echo of the bird’s call via the
ground; alternatively, they may orientate with the help of
changes in the position of (calling) conspecifics. There are
many suggestions but few answers. To predict the optimal
behaviour of a migrating bird with regard to its flight path is
one thing, but we should of course also wonder with what
mechanisms and with what accuracy it can achieve this. For
instance, is the variation we observe in flight altitude (Bruderer
et al. 1995; M. Klaassen and H. Biebach, in preparation) a
result of the inability of migrants to find the optimal altitude
for migration, or does it reflect inter- and intraspecific
variations in optimal flight altitude?
Conclusions
Despite painstaking and highly praiseworthy work
conducted by physiologists on flying birds (e.g. Tucker, 1966,
1968; Berger et al. 1971; Bernstein et al. 1973; Butler et al.
1977; Torre-Bueno 1978; Rothe et al. 1987), there is little
information on how water, energy and protein balance vary
with flight speed, altitude, humidity, ambient temperature and
the bird’s body mass. Much of what we use in models for
predicting and explaining the behaviour of migrating birds is
based on aerodynamic theory or extrapolated from
measurements of birds at rest instead of flying. More empirical
data are required and they should be assessed within a sound
theoretical framework. The migratory journey not only entails
flight but also stop-overs, where fuel loads are replenished. For
a proper understanding of migratory behaviour, both migratory
flight and refuelling should be integrated. In addition, in
explaining the behaviour and physiological design of migrants,
one should perhaps be more prudent in assuming that a bird’s
sensory ability is perfect during migratory flight; the
Metabolic constraints on long-distance migration in birds
physiological safety margins of migrants are probably closely
related to their navigational skills.
I gratefully acknowledge the valuable comments of Kenneth
Able, Ebo Gwinner, William Harvey, Miriam Lehrer, Åke
Lindström, Theunis Piersma and Sandra Ray on the
manuscript.
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